The Extended Phenotype

The Long Reach of the Gene

Not Your Parents' Web of Life

In the 19th century, Thomas Huxley was known as "Darwin's bull-dog" for his
active and tenacious defense of Darwinism. Richard Dawkins fills a similar
niche today, only with much more force and much less reserve about calling a
spade a shovel --- he's Darwin's pit-bull, not his bull-dog. Books like
The Blind Watchmaker and Climbing Mount Improbable do
an immense amount of good in the world, and I've seen them turn the
minds of many readers inside out. But they also lead to the reasonable
suspicion that Dawkins doesn't have much to offer those who accept what are,
after all, the elementary facts of life. By Dawkins's own reckoning, his most
important book is this one, and he's right. It gives what is at once
the most forceful and the most considered presentation of his distinctive
ideas, and it contain a genuinely important and novel concept derived from
them, namely that of the extended phenotype itself.

It is only fitting, then, that this epitome of Dawkins opens with one of the
most impressive refutations of genetic determinism I have encountered, at least
as powerful as any Stephen Jay Gould or Richard Lewontin has ever produced.
Genes do not determine anatomy or physiology or behavior; genes encode the
information to make proteins. Which genes will be expressed --- decoded into
proteins --- depends on a very subtle biochemical process, the complexity and
intricacy of which is hidden by the labels "signal transduction" and
"genetic regulation". The idea that, once we know an organism's genotype ---
have a complete inventory of its genes --- we could read off its traits is a
baseless fantasy propagated by people who are at best idiots (science
journalists, movie writers, newspaper editors, professional futurists), or at
worst should know much better (science fiction novelists, some molecular
biologists involved in the Human Genome Project).

What then is the sense of speaking of a gene for a trait, as competent
evolutionists and geneticists do all the time? Essentially, it's a statistical
claim about causation. A gene X is "for" a trait Y if and only if different
versions of X --- different alleles of X --- lead to differences in the
distribution of Y, in a particular context of other genes and environmental
factors. We can de-relativize this either by taking that context as more or
less fixed, or by saying that X is for Y if there is any context in which
differences in X lead to differences in Y. Now, this statement does not commit
us to the genetic determination of Y, at least not in any sane sense of
"determination". In particular, it is not a claim that:

Y is set in any very direct, chemical way by the protein X codes for;

the range of variation in Y, for a fixed allele at X, is small;

no other gene influences Y;

X influences no other trait;

changes in environmental factors can do little or nothing to change
Y;

the relation between X and Y has had any evolutionary importance.

A gene-centered view of evolution does not depend on any of these things.
All that the view needs are the facts that (1) genes are capable of statistical
influence on traits; (2) some of those traits influence reproductive success;
(3) genes pass mostly intact through reproduction --- they are high-fidelity
replicators; (4) other things --- genomes, whole organisms, groups of
organisms, species --- do not satisfy these constraints. Now, (1)--(3) are
certainly true, and not in dispute among those with their heads plugged in. It
is not hard --- now --- to see that the conjunction of these premises will lead
to an increase in the relative frequency of replicators which --- in the
context of other replicators and environmental contingencies --- produce traits
which have tended to aid reproductive success in the past. That is, there will
be selection for genes which act as if they were interested in
increasing their representation in future generations, as if they
pursued selfish genetic interests, as if genes wanted to make more genes in
their image, and produced "vehicles" which serve that end. I will henceforth
speak about genes making organisms do things which serve the genes' interests,
with the understanding that these metaphors can all be replaced, at the price
of tedium, with non-metaphorical statements about the statistical effects on
representation in future generations of allelic differences in a given
genetic-environmental context (a disclaimer which itself illustrates the use of
the metaphors).

The real controversy is in the claim (4), that organisms, groups and species
are not replicators, or at least not evolvable replicators. Groups can produce
more groups, and species can produce more species, just as genes can produce
more genes; does a process analogous to gene natural selection act on these
levels? This is an empirical issue, not an a priori one. Do these putative
replicators have a strong influence on traits which themselves have a strong
influence on reproductive success? That is, are these other replicators under
strong selection pressure? Is the copying fidelity of these replicators high?
The stronger the selection pressure, the sloppier replication can be and still
support natural selection. Is selection acting at these levels strong enough
to overcome the effects of gene selection and random drift? It seems that
groups, species, etc., are both under very weak selection pressure and very
sloppy replicators. But, as I said, genes are under strong selection pressure and are high-fidelity replicators; selection on genes, therefore, rules.

This leaves open the question of whether, in some circumstances, selection
might favor genes which, while deleterious to their carriers, benefit other
members of their group, even without kin selection (on which see below). It's
been shown --- for instance by John Pepper and
Barbara Smuts --- that this is possible, but I don't think we know whether
it's important in nature. This is sometimes also called "group selection,"
but I think that should be reserved for theories in which groups replicate.

One consequence of taking the gene's-eye-view is that we should expect the
versions of genes which encounter each other often --- the most common alleles
in the gene pool --- to be ones which are well-adapted to each other; indeed,
co-adapted. That is, genes will be selected to have consequences favorable to
their own reproduction in the presence of common alleles. (There's a clear
route from here to evolutionary game theory and evolutionarily stable
strategies.) This does not mean that they will be mutually supportive,
however. Rabbit genes will tend to adapt to a context partially determined by
which genes are common among foxes, and vice versa: hence evolutionary arms
races, on which Dawkins is (as usual) particularly acute.

Genes are selfish; if one can prosper replicatively at the expense of
others, it will do so. Normally, organisms have fairly elaborate machinery
which ensure that either all their genes get reproduced or none of them do;
this puts all their genes in the same boat, and encourages their cooperation.
It also, however, gives a serious advantage to any gene which can subvert that
machinery in its own favor. (Variants which muck with the machinery to their
detriment are, obviously, not long for this world.) There is considerable
evidence (reviewed here) that such extra-selfish genes are actually fairly
common, and somewhat less evidence that they do not completely dominate natural
populations because all genes not linked to the "outlaws" will be selected to
modify and inhibit their effects --- the "parliament of genes" effect.

Not only can genes within a single body compete, but genes in different
bodies can collaborate. The most familiar example of this is kin selection,
the phenomenon encapsulated in Haldane's joke that he would "lay down his life
for two brothers or eight cousins." That is, a gene might find it in its
interest to make the body it is in do things which depress its reproductive
prospects, if by doing so it raises those of other bodies which contain the
gene. In fact, if the benefits to the other bodies are sufficiently large in
relation to the costs, it makes sense for the gene to do this even if the other
bodies only probably contain the gene.

Mention of kin selection brings up the problem of "fitness". Many readers
will be surprised to learn that Dawkins thinks it is a not particularly useful
term, and one which evolutionist would probably be better off discarding. In
his ch. 10, "An Agony in Five Fits," he distinguishes no less than five
senses in which the term is used, only one of them (the fitness of a genotype
in population genetics) reasonably useful and operational. This is probably
the most technically involved chapter of the book, but also one of the most
important in driving home the point that selection really does act on genes,
the true replicators, and nothing else. This concludes the critical and as it
were dissecting portion of the book; having convinced his readers that genes
are what matters, he now (like the good reductionist that he is) proceeds to
show how they interact with each other to give us the phenomena we know and
love, or at least suffer through. Some of this work has actually already been
done, in the way of looking at arms-races, the co-adaptation of genes in a
common gene pool, and so forth. But the consequences of having genes interact
are, literally, much more far-ranging.

The phenotype of an organism is the collection of all its "manifested
attributes" --- a clear enough notion, if one difficult to make metaphysically
precise. The phenotype is the joint product of the genotype and the
environment. The original and important point Dawkins makes under the label of
"the extended phenotype" is that there is no good reason to suppose
that the phenotype stops at the skin (or bark or what-not), and that there are
many aspects of life which we can account for straightforwardly if only we
suppose that it does not. Dawkins starts modestly and plausibly enough with
the effects an organism has on its inanimate environment. Many animals make
artifacts --- shells, burrows, stores, and what-not --- which are subject to
genetic variation, and there seems to be no principled reason not to regard the
relevant genes as being "for" those artifacts, just as other genes are for
bodily traits. If variation in the artifacts in turn effects reproductive
success, then those genes will, in fact, be exposed to natural selection in the
ordinary way. (So far as I can recall, all of Dawkins's examples are of animal
behavior, but I don't see why we shouldn't expect plants, bacteria and the like
to have extended phenotypes as well. A tree which by increasing shade on the
forest floor inhibits the growth of rival plants would be a simple example.)

What is even more interesting is that Dawkins shows how the same mechanisms
can work even in the case of artifacts which are the joint work of many
animals.

Beaver dams and termite mounds are collectively built by the
behavioural efforts of more than one individual. A genetic mutation in one
individual beaver could show itself in phenotypic change in the shared
artefact. If the phenotypic change in the artefact had an influence on the
success of replication of the new gene, natural selection would act, positively
or negatively, to change the probability of similar artefacts existing in the
future. The gene's extended phenotypic effect, say an increase in the height
of the dam, affects its chances of survival precisely in the same sense as in
the case of a gene with a normal phenotypic effect, such as an increase in the
length of the tail. The fact that the dam is the shared product of the
building behaviour of several beavers does not alter the principle: genes that
tend to make beavers build high dams will themselves, on average, tend to reap
the benefits (or costs) of high dams, even though every dam may be jointly
built by several beavers. If two beavers working on the same dam have
different genes for dam height, the resulting extended phenotype will reflect
the interaction between the genes, in the same way as bodies reflect gene
interactions. There could be extended genetic analogues of epistasis, of
modifier genes, even of dominance and recessiveness. [p. 209]

In fact, Dawkins even shows that genes for a common extended-phenotypic
trait can be spread over several species, even over several kingdoms, without
messing up the mechanism of their evolution.

The next step is to go from phenotypes which are produced by several bodies
to phenotypes in other bodies. The most obvious case is that of
parasites altering the behavior of their hosts. This gives Dawkins a multitude
of bizarre examples of body-snatching, in which he plainly revels; but the
subject is also of great importance to medicine,
where we want to know, before trying to suppress a symptom, whether it is the
host's way of combating the parasite, or on the contrary something the parasite
makes the host do to the parasite's advantage. Having been lulled by the
parasites, the reader is prepared to see extended-phenotypic manipulations all
over the place: between parents and offspring, for instance (in either
direction), or between siblings (in eusocial insects, for instance); the field
of animal communication as a whole begins to look like an extended exercise in
indirect mind-control. Dawkins is at length led to the following thesis: "An
animal's behaviour tends to maximize the survival of the genes 'for' that
behaviour, whether or not those genes happen to be in the body of the
particular animal performing it" (p. 233). Do not be misled by fact that this
sentence is in the indicative; it is really a recommendation to look for genes
which benefit from behaviors, whether they happen to be in the same body or
not, and not a statement that, as a matter of fact, there are always such genes
(cf. ch. 3, "Constraints on Perfection").

Ultimately, Dawkins presents a vision of the organic world and its
appurtenances as overlapping fields of power exerted by replicators over each
other and over the vehicles which they construct to carry themselves into
future generations. Replicators, moreover, are fully capable of (as Dawkins
puts it) "action at a distance," and potentially immense distances in both
space and time, by quite subtle routes. It is a tough-minded vision, deeply at
odds with the view that nature is naturally cooperative and harmonious, except
where we've mucked it up --- the view that Dawkins, with his usual accurate
scorn, calls "the BBC Theorem". The web of genetic control and
interdependence is as vast, subtle and far-reaching as that invoked by the BBC
Theorem, but immeasurably less nice, allowing both cooperation and competition,
as the interests of the genes dictate. (I shall refrain from pointing out the
similarities between this vision and that of Foucault, since that would merely
cause indignation all around.)

The last chapter is devoted to the question of why, given this vision of
replicative action-at-a-distance, life should come bundled into discrete
organisms at all. Passing on the question of why we have cells, Dawkins turns
to the problem of why multicellular organisms should exist, and why they should
all go through a stage where they consist of a single cell which then
multiplies and differentiates. He presents an ingenious argument, derived from one put forth by by the developmental
biologist John Tyler Bonner, as to why this "bottle-neck" facilitates the
evolution of complex adaptations, in ways that simple growth would not. This
doesn't guarantee such bottlenecks will evolve, but shifts the problem to the
more tractable one of why they do so. (The latest views on this have been
summarized by Maynard Smith and
Szathmáry, as constant readers will recall.)

This is a technical and controversial work addressed to Dawkins's fellow
biologists; it is also enviably, relentlessly clear, both in its prose and its
logic. This is writing like a spear: a hard, sharp point, everything needed to
drive the point home, and nothing else. Inevitably it needs more background
than a book like The Blind Watchmaker, but it can be
followed by those whose knowledge of evolutionary biology is entirely at the
level of popular works. I strongly urge everyone with that preparation to read
this book, not only to encounter an important, coherent view of evolution, but
simply to see what can be done with words and ideas in the hands of a master.

Disclaimer: I didn't ask for a review copy of this book, but the
publishers sent me one anyway. Needless to say, I have no stake in its
success.
x + 313 pp., glossary, bibliography, "further reading" (= selected
relevant works which have appeared since 1982), author and subject indices
Evolution /
GeneticsCurrently in print as a paperback, US$16.95, ISBN 0-19-288051-9 [Buy
from Powell's]. Apart from the "further reading" and the afterword, this
edition is identical to the edition of 1989, which in turn differed from that
of 1982 only in the subtitle, and in the addition of two paragraphs to the
preface.
25 February 2000
Thanks to John Pepper for a pre-print copy of his paper and helpful
discussions, and to Danny Yee for pointing out an obscurity.